bs_bs_banner Zoological Journal of the Linnean Society, 2014, 170, 779–821. With 13 figures The characters of Palaeozoic jawed vertebrates MARTIN D. BRAZEAU1* and MATT FRIEDMAN2 1Naturalis Biodiversity Center, P.O. Box 9514, 2300 RA Leiden, The Netherlands 2Department of Earth Sciences, University of Oxford, South Parks Road, Oxford OX1 3AN, UK Received 14 June 2013; revised 27 October 2013; accepted for publication 30 October 2013 Newly discovered fossils from the Silurian and Devonian periods are beginning to challenge embedded perceptions about the origin and early diversification of jawed vertebrates (gnathostomes). Nevertheless, an explicit cladistic framework for the relationships of these fossils relative to the principal crown lineages of the jawed vertebrates (osteichthyans: bony fishes and tetrapods; chondrichthyans: sharks, batoids, and chimaeras) remains elusive. We critically review the systematics and character distributions of early gnathostomes and provide a clearly stated hierarchy of synapomorphies covering the jaw-bearing stem gnathostomes and osteichthyan and chondrichthyan stem groups. We show that character lists, designed to support the monophyly of putative groups, tend to overstate their strength and lack cladistic corroboration. By contrast, synapomorphic hierarchies are more open to refutation and must explicitly confront conflicting evidence. Our proposed synapomorphy scheme is used to evaluate the status of the problematic fossil groups Acanthodii and Placodermi, and suggest profitable avenues for future research. We interpret placoderms as a paraphyletic array of stem-group gnathostomes, and suggest what we regard as two equally plausible placements of acanthodians: exclusively on the chondrichthyan stem, or distributed on both the chondrichthyan and osteichthyan stems. © 2014 The Authors. Zoological Journal of the Linnean Society published by John Wiley & Sons Ltd on behalf of The Linnean Society of London, Zoological Journal of the Linnean Society, 2014, 170, 779–821. doi: 10.1111/zoj.12111 ADDITIONAL KEYWORDS: Acanthodii – Chondrichthyes – Gnathostomata – morphology – Osteichthyes – palaeontology – Placodermi – plesiomorphy – synapomorphy. [T]he evidence from all useful characters must be weighed of living taxa. Instead, the problems surround the impartially, and unbiased comparisons must be made with all placement of fossil taxa with respect to the modern potentially related groups. groups. Gnathostomes are divided into two extant R. Denison (1979: 19). lineages: the Chondrichthyes (sharks, rays and skates, and chimaeras) and much more diverse INTRODUCTION Osteichthyes (bony fishes and tetrapods). That these are sister groups and reciprocally monophyletic is The phylogenetic relationships of early fossil not greatly disputed, and is well supported by both gnathostomes (jawed vertebrates) remains one of the molecular and morphological studies (Nelson, 1969; most significant but under-researched problems in Wiley, 1979; Maisey, 1986; Takezaki et al., 2003; Blair vertebrate palaeontology. Unlike many other areas of & Hedges, 2005; Chen et al., 2012). Debate currently vertebrate systematics, the debates do not concern concerns the phylogenetic placement and monophyly how fossils might illuminate the inter-relationships of two exclusively fossil assemblages: the placoderms, armoured fishes with simple jaws and dental struc- tures that are hotly debated homologues of teeth, and *Corresponding author. Current address: Department of Life the acanthodians, shark-like fishes with numerous Sciences, Imperial College London, Silwood Park Campus, Buckhurst Road, Ascot SL5 7PY, UK. bony spines preceding their fins. When gnathostome E-mail: [email protected] fossils cannot be placed in either of the extant groups © 2014 The Authors. Zoological Journal of the Linnean Society published by John Wiley & Sons Ltd 779 on behalf of The Linnean Society of London, Zoological Journal of the Linnean Society, 2014, 170, 779–821 This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made. 780 M. D. BRAZEAU AND M. FRIEDMAN they have typically been assigned to either of these These include the relative order of appearance of extinct categories. From a phylogenetic perspective, features such as an epicercal tail, paired pectoral that leaves few fossil branches that can be used to appendages, and perichondral bone (Forey & Janvier, infer sequences of character acquisition in important 1993; Janvier, 1996a; Donoghue et al., 2000; Janvier, parts of the gnathostome tree, such as those that 2001; Gai et al., 2011). document the origin of jaws and the unique anatomi- By comparison, the application of cladistic methods cal attributes of chondrichthyans and osteichthyans. to the early gnathostome problem is in a state of Although fossils of Devonian and Silurian fishes infancy. This relative lack of progress is paradoxical: that challenge old perceptions are frequently coming early gnathostome fossils are similarly diverse as their to light (Zhu, Yu & Janvier, 1999; Maisey, 2001; jawless counterparts and almost certainly richer in Maisey & Anderson, 2001; Miller, Cloutier & Turner, characters. Only a few numerical cladistic analyses 2003; Hanke & Wilson, 2004, 2006, 2010; Brazeau, have had the taxonomic scope to test such fundamental 2009; Maisey, Miller & Turner, 2009; Zhu et al., 2009, phylogenetic questions as the monophyly of placo- 2012a, 2013), comparatively little effort has been derms and acanthodians, and evaluate competing spent to investigate their phylogenetic relationships. placements for stem members of Osteichthyes, Chon- In addition to this, the record of even the earliest drichthyes, and Gnathostomata (Friedman, 2007a; jawed vertebrates is characterized by considerable Brazeau, 2009; Davis et al., 2012; Zhu et al., 2013). In anatomical disparity (Anderson et al., 2011; Davis, this paper, we elaborate on the body of character Finarelli & Coates, 2012). Currently, placoderms information emerging from these recent analyses. We are the only group of widely accepted stem-group explore conflicting data, and frame the relevant sys- gnathostomes that are known to exhibit jaws (Young, tematic questions, as we see them, with greater explic- 1986). Acanthodians have been placed in this position itness, and set clear avenues for future research. To do at one time or another (Watson, 1937; Rosen et al., this, we address three fundamental problems: 1981; Brazeau, 2009; Davis et al., 2012), but this has 1. How might previous palaeontological collection, rarely been consistent and the character support is research, and analysis have failed to populate unclear. Meanwhile, fossils that branch between the naked stem-group branches of the chondrich- placoderms and their nearest jawless relatives have thyan, osteichthyan, and crownward parts of the yet to be discovered or identified. Consequently no gnathostome stem (Fig. 1)? anatomical intermediates are known to punctuate 2. What are the principal characters describing the this conspicuous gap. The number of stem osteich- hierarchy of these three gnathostome branches thyans and stem chondrichthyans identified with incident to the gnathostome crown node? any confidence is similarly limited, with candidates 3. What are the implications of the resulting scheme usually sourced from the acanthodians. Nevertheless, for interpreting problematic or unusual taxa? the fossils of early gnathostomes are sometimes used as background for hypotheses of character and devel- To address these questions, we need to re-evaluate opmental evolution, even though these relationships the phylogenetic status of the two main extinct groups, and character transformations remain unclear (e.g. placoderms and acanthodians, through a critical Beverdam et al., 2002; Koentges & Matsuoka, 2002; examination of their characters. As in our previous Gillis et al., 2011). work on osteichthyans (Friedman & Brazeau, 2010), Over the past three decades, pioneering cladistic we can assess whether our current systematic tradi- work has made it clear that Palaeozoic armoured tions may be causing us to misidentify or misinterpret jawless fishes, sometimes called ‘ostracoderms’, are a fossils. We feel the best approach to the problem is paraphyletic array of stem gnathostomes (Janvier, captured by Denison’s (1979) quote in the epigraph. 1981a, 1984; Forey & Janvier, 1993). This brought Denison invites us to make comparisons not just an end to decades of work that considered the within the groups that we have inherited by the ‘ostracoderms’ almost exclusively in light of them- traditions of our discipline, but to compare each selves (see review in Janvier, 1996b), and intro- one objectively and across the perceived taxonomic duced a computational framework for studying boundaries as though they did not exist at all. In this stem gnathostome relationships (Donoghue, Forey & way, we can better establish the quality of evidence Aldridge, 2000). Although uncertainty and disagree- that forms the basis of our current systematics of early ment remains about the precise relationships of gnathostomes. jawless stem gnathostomes, debates on the topic have proved highly fruitful. The resulting synapomorphic hierarchies have elucidated the step-wise acquisition A HISTORY OF THE ‘PLACODERM PROBLEM’ of a suite of anatomical features